► Trace metal toxicity is not typically directly related to total accumulated body concentration. ► Trace metal toxicity is related to total rate of trace metal uptake. ► Trace metal toxicity is ...related to a critical concentration of metabolically available metal. ► Critical concentration of metabolically available zinc in a crustacean is estimated as 150
μg
g
−1.
We use published data on the different patterns of the bioaccumulation of zinc by three crustaceans, the caridean decapod
Palaemon elegans, the amphipod
Orchestia gammarellus and the barnacle
Amphibalanus amphitrite, to construct comparative biodynamic models of the bioaccumulation of zinc into metabolically available and detoxified components of accumulated zinc in each crustacean under both field and laboratory toxicity test conditions. We then link these bioaccumulation models to the onset of toxic effects on exposure of the crustaceans to high dissolved zinc bioavailabilities, using the tenets that toxicity effects are related to the total uptake rate of the toxic metal, and that toxicity is not usually dependent on the total accumulated metal concentration but always on the concentration of accumulated metal that is metabolically available. We dismiss the general concept that there is a critical accumulated body concentration of a metal in an invertebrate at which toxicity ensues, except under specific circumstances involving a rare lack of storage detoxification of accumulated metal. We thus propose a theoretical framework that can be extended to other metals and other aquatic invertebrates (indeed other animals) to explain the variation in the relationship between bioaccumulated body concentrations and toxicity, and subsequently to predict this relationship in many other species for which we have bioaccumulation modelling data.
Many aspects of metal accumulation in aquatic invertebrates (i.e. toxicity, tolerance and trophic transfer) can be understood by examining the subcellular partitioning of accumulated metal. In this ...paper, we use a compartmentalization approach to interpret the significance of metal, species and size dependence in the subcellular partitioning of Cd and Zn in the bivalvesMacoma balthicaandPotamocorbula amurensis. Of special interest is the compartmentalization of metal as metal-sensitive fractions (MSF) (i.e. organelles and heat-sensitive proteins, termed ‘enzymes’ hereafter) and biologically detoxified metal (BDM) (i.e. metallothioneins MT and metal-rich granules MRG). Clams from San Francisco Bay, CA, were exposed for 14 d to seawater (20‰ salinity) containing 3.5 μg l–1Cd and 20.5 μg l–1Zn, including109Cd and65Zn as radiotracers. Uptake was followed by 21 d of depuration. The subcellular partitioning of metal within clams was examined following exposure and loss.P. amurensisaccumulated ~22× more Cd and ~2× more Zn thanM. balthica. MT played an important role in the storage of Cd inP. amurensis, while organelles were the major site of Zn accumulation. InM. balthica, Cd and Zn partitioned similarly, although the pathway of detoxification was metal-specific (MRG for Cd; MRG and MT for Zn). Upon loss,M. balthicadepurated ~40% of Cd with Zn being retained;P. amurensisretained Cd and depurated Zn (~40%). During efflux, Cd and Zn concentrations in the MSF compartment of both clams declined with metal either being lost from the animal or being transferred to the BDM compartment. Subcellular compartmentalization was also size-dependent, with the importance of BDM increasing with clam size; MSF decreased accordingly. We hypothesized that progressive retention of metal as BDM (i.e. MRG) with age may lead to size dependency of metal concentrations often observed in some populations ofM. balthica.
Ecological risks from metal contaminants are difficult to document because responses differ among species, threats differ among metals, and environmental influences are complex. Unifying concepts are ...needed to better tie together such complexities. Here we suggest that a biologically based conceptualization, the biodynamic model, provides the necessary unification for a key aspect in risk: metal bioaccumulation (internal exposure). The model is mechanistically based, but empirically considers geochemical influences, biological differences, and differences among metals. Forecasts from the model agree closely with observations from nature, validating its basic assumptions. The biodynamic metal bioaccumulation model combines targeted, high-quality geochemical analyses from a site of interest with parametrization of key physiological constants for a species from that site. The physiological parameters include metal influx rates from water, influx rates from food, rate constants of loss, and growth rates (when high). We compiled results from 15 publications that forecast species-specific bioaccumulation, and compare the forecasts to bioaccumulation data from the field. These data consider concentrations that cover 7 orders of magnitude. They include 7 metals and 14 species of animals from 3 phyla and 11 marine, estuarine, and freshwater environments. The coefficient of determination (R 2) between forecasts and independently observed bioaccumulation from the field was 0.98. Most forecasts agreed with observations within 2-fold. The agreement suggests that the basic assumptions of the biodynamic model are tenable. A unified explanation of metal bioaccumulation sets the stage for a realistic understanding of toxicity and ecological effects of metals in nature.
This paper examines how the subcellular partitioning of Cd and Zn in the bivalvesMacoma balthicaandPotamocorbula amurensismay affect the trophic transfer of metal to predators. Results show that the ...partitioning of metals to organelles, ‘enzymes’ and metallothioneins (MT) comprise a subcellular compartment containing trophically available metal (TAM; i.e. metal trophically available to predators), and that because this partitioning varies with species, animal size and metal, TAM is similarly influenced. Clams from San Francisco Bay, California, were exposed for 14 d to 3.5 μg l–1Cd and 20.5 μg l–1Zn, including109Cd and65Zn as radiotracers, and were used in feeding experiments with grass shrimpPalaemon macrodatylus, or used to investigate the subcellular partitioning of metal. Grass shrimp fed Cd-contaminatedP. amurensisabsorbed ~60% of ingested Cd, which was in accordance with the partitioning of Cd to the bivalve’s TAM compartment (i.e. Cd associated with organelles, ‘enzymes’ and MT); a similar relationship was found in previous studies with grass shrimp fed Cd-contaminated oligochaetes. Thus, TAM may be used as a tool to predict the trophic transfer of at least Cd. Subcellular fractionation revealed that ~34% of both the Cd and Zn accumulated byM. balthicawas associated with TAM, while partitioning to TAM inP. amurensiswas metal-dependent (~60% for TAM-Cd%, ~73% for TAM-Zn%). The greater TAM-Cd% ofP. amurensisthanM. balthicais due to preferential binding of Cd to MT and ‘enzymes’, while enhanced TAM-Zn% ofP. amurensisresults from a greater binding of Zn to organelles. TAM for most species–metal combinations was size-dependent, decreasing with increased clam size. Based on field data, it is estimated that of the 2 bivalves,P. amurensisposes the greater threat of Cd exposure to predators because of higher tissue concentrations and greater partitioning as TAM; exposure of Zn to predators would be similar between these species.
Arsenic bioaccumulation in the deposit-feeding polychaete
Arenicola marina has been investigated using biodynamic modelling. Radiotracer techniques were used to determine the rates of uptake of As as ...arsenate from water and sediment and its subsequent efflux in the laboratory. Lugworms accumulated As from solution linearly at concentrations of 2–20
μg
l
−1, with a corresponding uptake rate constant of 0.1648
±
0.0135
l
g
−1
d
−1. 7.8
±
0.8% (assimilation efficiency) of the As ingested bound to sediments was retained after egestion of unassimilated metal. Elimination of As followed a two-compartment model, with mean efflux rate constants (from the slow pool) very similar for As accumulated from solution and ingested sediments (0.0449
±
0.0034 and 0.0478
±
0.0225
d
−1, respectively) and a corresponding biological half-time of roughly 15
d. A biodynamic model was constructed and validated through the comparison of biodynamic model predictions against measured bioaccumulated concentrations in lugworms from five UK estuaries. The model accurately predicted bioaccumulated As concentrations in lugworms using mean values of relevant physiological parameters (uptake rate, efflux rate and growth rate constants), a site-specific ingestion rate (calculated according to mean worm size and sediment organic matter content and expressed as the rate of ingestion of the mass of fine sediment), a site-specific sediment concentration measured after HCl extraction, and a standard dissolved As concentration. This combination of parameters showed that sediment ingestion contributed 30–60% of the total As accumulated by lugworms at the studied sites, depending on the different geochemistry at each site. This study showed that it is difficult to predict accurately As bioaccumulation at sites with different chemistries, unless that chemistry is taken into account.
Many estuaries of southwest England were heavily contaminated with toxic metals associated with the mining of copper and other metals, particularly between 1850 and 1900. The question remains whether ...the passage of time has brought remediation to these estuaries. In 2003 and 2006 we revisited sites in 5 metal-contaminated estuaries sampled in the 1970s and 1980s — Restronguet Creek, Gannel, West Looe, East Looe and Tavy. We evaluate changes in metal contamination in sediments and in metal bioavailabilities in sediments and water to local organisms employed as biomonitors. We find that the decline in contamination in these estuaries is complex. Differences in bioavailable contamination in the water column were detectable, as were significant detectable changes in at least some estuaries in bioavailable metal contamination originating from sediments. However, in the 100years since mining activities declined, bioavailable contamination has not declined to the regional baseline in any estuary affected by the mine wastes. The greatest decline in contamination occurred in the one instance (East Looe) where a previous industrial source of (Ag) contamination was considered. We used the macroalgae Fucus vesiculosus and Ascophyllum nodosum as biomonitors of dissolved metal bioavailabilities and the deposit feeders Nereis diversicolor and Scrobicularia plana as biomonitors of bioavailable metal in sediments. We found no systematic decrease in the atypically high Ag, Cu, Pb and Zn concentrations in the estuarine sediments over a 26year period. Accumulated metal (Ag, As, Cu, Pb, and Zn) concentrations in the deposit feeders are similarly still atypically high in at least one estuary for each metal, and there is no consistent evidence for general decreases in sediment metal bioavailabilities over time. We conclude that the legacy of mining in sheltered estuaries of southwest England is the ongoing presence of sediments rich in metals bioavailable to deposit feeders, while dissolved metal bioavailabilities from this historical source alone are no longer atypically high.
► SW England estuaries are contaminated with toxic metals from historical mining. ► High metal concentrations remain in the sediments. ► High metal concentrations still in biomonitors of sediment contamination. ► Mining legacy is sediments rich in metals bioavailable to deposit feeders. ► Bioavailabilities of dissolved metals from historical mining are no longer high.
Aquatic insects often dominate lotic ecosystems, yet these organisms are under-represented in trace metal toxicity databases. Furthermore, toxicity data for aquatic insects do not appear to reflect ...their actual sensitivities to metals in nature, because the concentrations required to elicit toxicity in the laboratory are considerably higher than those found to impact insect communities in the field. New approaches are therefore needed to better understand how and why insects are differentially susceptible to metal exposures. Biodynamic modeling is a powerful tool for understanding interspecific differences in trace metal bioaccumulation. Because bioaccumulation alone does not necessarily correlate with toxicity, we combined biokinetic parameters associated with dissolved cadmium exposures with studies of the subcellular compartmentalization of accumulated Cd. This combination of physiological traits allowed us to make predictions of susceptibility differences to dissolved Cd in three aquatic insect taxa: Ephemerella excrucians, Rhithrogena morrisoni, and Rhyacophila sp. We compared these predictions with long-term field monitoring data and toxicity tests with closely related taxa: Ephemerella infrequens, Rhithrogena hageni, and Rhyacophila brunea. Kinetic parameters allowed us to estimate steady-state concentrations, the time required to reach steady state, and the concentrations of Cd projected to be in potentially toxic compartments for different species. Species-specific physiological traits identified using biodynamic models provided a means for better understanding why toxicity assays with insects have failed to provide meaningful estimates for metal concentrations that would be expected to be protective in nature.
The groundwater in a shallow, unconfined, low-lying coastal aquifer in Santala, southern Finland, was chemically characterised by integrating multivariate statistical approaches, principal component ...analysis (PCA) and hierarchical cluster analysis (HCA), based on the stable isotopes δ2H and δ18O, hydrogeochemistry and field monitoring data. PCA and HCA yielded similar results and classified groundwater samples into six distinct groups that revealed the factors controlling temporal and spatial variations in the groundwater geochemistry, such as the geology, anthropogenic sources from human activities, climate and surface water. High temporal variation in groundwater chemistry directly corresponded to precipitation. With an increase in precipitation, KMnO4 consumption, EC, alkalinity and Ca concentrations also increased in most wells, while Fe, Al, Mn and SO4 were occasionally increased during spring after the snowmelt under specific geological conditions. The continued increase in NO3 and metal concentrations in groundwater indicates the potential contamination risk to the aquifer. Stable isotopes of δ18O and δ2H indicate groundwater recharge directly from meteoric water, with an insignificant contribution from lake water, and no seawater intrusion into the aquifer. Groundwater geochemistry suggests that local seawater intrusion is temporarily able to take place in the sulfate reduction zone along the freshwater and seawater mixed zone in the low-lying coastal area, but the contribution of seawater was found to be very low. The influence of lake water could be observed from higher levels of KMnO4 consumption in wells near the lake. The integration of PCA and HCA with conventional classification of groundwater types, as well as with the hydrogeochemical data, provided useful tools to identify the vulnerable groundwater areas representing the impacts of both natural and human activities on water quality and the understanding of complex groundwater flow system for the aquifer vulnerability assessment and groundwater management in the future.
We conducted a study with cadmium (Cd) and copper (Cu) in the delta of San Francisco Bay, using nitrogen and carbon stable isotopes to identify trophic position and food web structure. Cadmium is ...progressively enriched among trophic levels in discrete epiphyte-based food webs composed of macrophyte-dwelling invertebrates (the first link being epiphytic algae) and fishes (the first link being gobies). Cadmium concentrations were biomagnified 15 times within the scope of two trophic links in both food webs. Trophic enrichment in invertebrates was twice that of fishes. No tendency toward trophic-level enrichment was observed for Cu, regardless of whether organisms were sorted by food web or treated on a taxonomic basis within discrete food webs. The greatest toxic effects of Cd are likely to occur with increasing trophic positions, where animals are ingesting Cd-rich prey (or food). In Franks Tract this occurs within discrete food chains composed of macrophyte-dwelling invertebrates or fishes inhabiting submerged aquatic vegetation. Unraveling ecosystem complexity is necessary before species most exposed and at risk can be identified.
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